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Harmful algal blooms (HABs) of the toxic haptophytePrymnesium parvumare a recurrent problem in many inland and estuarine waters around the world. Strains ofP. parvumvary in the toxins they produce and in other physiological traits associated with HABs, but the genetic basis for this variation is unknown. To investigate genome diversity in this morphospecies, we generated genome assemblies for fifteen phylogenetically and geographically diverse strains ofP. parvumincluding Hi-C guided, near-chromosome level assemblies for two strains. Comparative analysis revealed considerable DNA content variation between strains, ranging from 115 Mbp to 845 Mbp. Strains included haploids, diploids, and polyploids, but not all differences in DNA content were due to variation in genome copy number. Haploid genome size between strains of different chemotypes differed by as much as 243 Mbp. Syntenic and phylogenetic analyses indicate that UTEX 2797, a common laboratory strain from Texas, is a hybrid that retains two phylogenetically distinct haplotypes. Investigation of gene families variably present across strains identified several functional categories associated with metabolism, including candidates for the biosynthesis of toxic metabolites, as well as genome size variation, including recent proliferations of transposable elements. Together, our results indicate thatP. parvumis comprised of multiple cryptic species. These genomes provide a robust phylogenetic and genomic framework for investigations into the eco-physiological consequences of the intra- and inter-specific genetic variation present inP. parvumand demonstrate the need for similar resources for other HAB-forming morphospecies.SIGNIFICANCE STATEMENTHarmful algal blooms (HABs) are a global concern. Efforts to understand the genetic basis of traits associated with the success of HAB-forming species are limited by a dearth of genomic resources. In this paper we present genomes for fifteen strains ofPrymnesium parvum, a toxic alga that causes ecosystem and societally disruptive HABs around the world. We uncover an unprecedented amount of sequence-level, gene family, and genome architecture evolution inP. parvumand provide evidence for both cryptic speciation and hybridization. These results illustrate how both inter- and intraspecific genetic variation can be dramatically underestimated in a protist morphospecies. More work is needed to understand the eco-physiological consequences of hidden genetic diversity inP. parvumand HAB-forming species more generally.

Programmed cell death (PCD) occurs in both unicellular and multicellular organisms. While PCD plays a key role in the development and maintenance of multicellular organisms, explaining why single-celled organisms would evolve to actively commit suicide has been far more challenging. Here, we explore the potential for PCD to act as an accessory to microbial bet-hedging strategies that utilize stochastic phenotype switching. We consider organisms that face unpredictable and recurring disasters, in which fitness depends on effective phenotypic diversification. We show that when reproductive opportunities are limited by carrying capacity, PCD drives population turnover, providing increased opportunities for phenotypic diversification through stochastic phenotype switching. The main cost of PCD, providing resources for growth to a PCD(-) competitor, is ameliorated by genetic assortment in spatially structured populations. Using agent -based simulations, we explore how basic demographic factors, namely bottlenecks and local dispersal, can generate sufficient spatial structure to favor the evolution of high PCD rates.

Programmed cell death (PCD) occurs in both unicellular and multicellular organisms. While PCD plays a key role in the development and maintenance of multicellular organisms, explaining why single-celled organisms would evolve to actively commit suicide has been far more challenging. Here, we explore the potential for PCD to act as an accessory to microbial bet-hedging strategies that utilize stochastic phenotype switching. We consider organisms that face unpredictable and recurring disasters, in which fitness depends on effective phenotypic diversification. We show that when reproductive opportunities are limited by carrying capacity, PCD drives population turnover, providing increased opportunities for phenotypic diversification through stochastic phenotype switching. The main cost of PCD, providing resources for growth to a PCD(-) competitor, is ameliorated by genetic assortment driven by population spatial structure. Using three dimensional agent based simulations, we explore how basic demographic factors, namely cell death and clonal reproduction, can create populations with sufficient spatial structure to favor the evolution of high PCD rates.

The evolution of multicellular life requires cooperation among cells, which can be undermined by intra-group selection for selfishness. Theory predicts that selection to avoid non-cooperators limits social interactions among non-relatives, yet previous evolution experiments suggest that intra-group conflict is an outcome, rather than a driver, of incipient multicellular life cycles. Here we report the evolution of multicellularity via two distinct mechanisms of group formation in the unicellular budding yeast Kluyveromyces lactis. Cells remain permanently attached following mitosis, giving rise to clonal clusters (staying together); clusters then reversibly assemble into social groups (coming together). Coming together amplifies the benefits of multicellularity and allows social clusters to collectively outperform solitary clusters. However, cooperation among non-relatives also permits fast-growing unicellular lineages to ‘free-ride' during selection for increased size. Cooperation and competition for the benefits of multicellularity promote the stable coexistence of unicellular and multicellular genotypes, underscoring the importance of social and ecological context during the transition to multicellularity., Multicellularity can arise by cells aggregating or remaining connected after cell division. Here, Driscoll and Travisano show that both mechanisms operate in experimentally evolved strains of the yeast Kluyveromyces lactis, with transient aggregation facilitating the coexistence of unicellular and multicellular genotypes.

Cooperation is fundamental to the survival of many bacterial species. Previous studies have shown that spatial structure can both promote and suppress cooperation. Most environments where bacteria are found are periodically disturbed, which can affect the spatial structure of the population. Despite the important role that spatial disturbances play in maintaining ecological relationships, it remains unclear as to how periodic spatial disturbances affect bacteria dependent on cooperation for survival. Here, we use bacteria engineered with a strong Allee effect to investigate how the frequency of periodic spatial disturbances affects cooperation. We show that at intermediate frequencies of spatial disturbance, the ability of the bacterial population to cooperate is perturbed. A mathematical model demonstrates that periodic spatial disturbance leads to a tradeoff between accessing an autoinducer and accessing nutrients, which determines the ability of the bacteria to cooperate. Based on this relationship, we alter the ability of the bacteria to access an autoinducer. We show that increased access to an autoinducer can enhance cooperation, but can also reduce ecological resistance, defined as the ability of a population to resist changes due to disturbance. Our results may have implications in maintaining stability of microbial communities and in the treatment of infectious diseases.

In recent years, sociobiology has been extended to microorganisms. Viewed through this lens, the microbial world is replete with cooperative behaviors. However, little attention has been paid to alternate hypotheses, making many studies self-confirming. Somewhat apart is a recent analysis of pyoverdin production-a paradigmatic public good and social trait-by Pseudomonas, which has revealed discord between predictions arising from sociobiology and the biology of microbes. This led the authors, Zhang and Rainey (Z&R), to question the generality of the conclusion that pyoverdin is a social trait, and to question the fit between the sociobiology framework and microbiology. This has unsettled Kummerli and Ross-Gillespie (K&R), who in a recent "Technical Comment" assert that arguments presented by Z&R are flawed, their experiments technically mistaken, and their understanding of social evolution theory naive. We demonstrate these claims to be without substance and show the conclusions of K&R to be based on a lack of understanding of redox chemistry and on misinterpretation of data. We also point to evidence of cherry-picking and raise the possibility of confirmation bias. Finally, we emphasize that the sociobiology framework applied to microbes is a hypothesis that requires rigorous and careful appraisal.

Biology needs a concept of individuality in order to distinguish organisms from parts of organisms and from groups of organisms, to count individuals and compare traits across taxa, and to distinguish growth from reproduction. Most of the proposed criteria for individuality were designed for ‘unitary’ or ‘paradigm’ organisms: contiguous, functionally and physiologically integrated, obligately sexually reproducing multicellular organisms with a germ line sequestered early in development. However, the vast majority of the diversity of life on Earth does not conform to all of these criteria. We consider the issue of individuality in the ‘minor’ multicellular taxa, which collectively span a large portion of the eukaryotic tree of life, reviewing their general features and focusing on a model species for each group. When the criteria designed for unitary organisms are applied to other groups, they often give conflicting answers or no answer at all to the question of whether or not a given unit is an individual. Complex life cycles, intimate bacterial symbioses, aggregative development, and strange genetic features complicate the picture. The great age of some of the groups considered shows that ‘intermediate’ forms, those with some but not all of the traits traditionally associated with individuality, cannot reasonably be considered ephemeral or assumed transitional. We discuss a handful of recent attempts to reconcile the many proposed criteria for individuality and to provide criteria that can be applied across all the domains of life. Finally, we argue that individuality should be defined without reference to any particular taxon and that understanding the emergence of new kinds of individuals requires recognizing individuality as a matter of degree.

The question of how altruism can evolve despite its local disadvantage to selfishness has produced a wealth of theoretical and empirical research capturing the attention of scientists across disciplines for decades. One feature that has remained consistent through this outpouring of knowledge has been that researchers have looked to the altruists themselves for mechanisms by which altruism can curtail selfishness. An alternative perspective may be that just as altruists want to limit selfishness in the population, so may the selfish individuals themselves. These alternative perspectives have been most evident in the fairly recent development of enforcement strategies. Punishment can effectively limit selfishness in the population, but it is not free. Thus, when punishment evolves among altruists, the double costs of exploitation from cheaters and punishment make the evolution of punishment problematic. Here we show that punishment can more readily invade selfish populations when associated with selfishness, whereas altruistic punishers cannot. Thereafter, the establishment of altruism because of enforcement by selfish punishers provides the ideal invasion conditions for altruistic punishment, effectively creating a transition of punishment from selfishness to altruistic. Thus, from chaotic beginnings, a little hypocrisy may go a long way in the evolution and maintenance of altruism.

Bacteria rely on a range of extracellular metabolites to suppress competitors, gain access to resources, and exploit plant or animal hosts. The GacS/GacA two-component regulatory system positively controls the expression of many of these beneficial external products in pseudomonad bacteria. Natural populations often contain variants with defective Gac systems that do not produce most external products. These mutants benefit from a decreased metabolic load but do not appear to displace the wild type in nature. How could natural selection maintain the wild type in the presence of a mutant with enhanced growth? One hypothesis is that Gac mutants are “cheaters” that do not contribute to the public good, favored within groups but selected against between groups, as groups containing more mutants lose access to ecologically important external products. An alternative hypothesis is that Gac mutants have a mutualistic interaction with the wild type, so that each variant benefits by the presence of the other. In the biocontrol bacterium Pseudomonas chlororaphis strain 30-84, Gac mutants do not produce phenazines, which suppress competitor growth and are critical for biofilm formation. Here, we test the predictions of these alternative hypotheses by quantifying interactions between the wild type and the phenazine- and biofilm-deficient Gac mutant within growing biofilms. We find evidence that the wild type and Gac mutants interact mutualistically in the biofilm context, whereas a phenazine-defective structural mutant does not. Our results suggest that the persistence of alternative Gac phenotypes may be due to the stabilizing role of local mutualistic interactions.

Organisms from prokaryotes to plants and animals make costly investments in diffusible beneficial external products. While the costs of producing such products are born only by the producer, the benefits may be distributed more widely. How are external goods-producing populations stabilized against invasion by nonproducing variants that receive the benefits without paying the cost? This question parallels the classic question of altruism, but because external goods production need not be altruistic per se, a broader range of conditions may lead to the maintenance of these traits. We start from the physics of diffusion to develop an expression for the conditions that favor the production of diffusible external goods. Important variables in determining the evolutionary outcome include the diffusion coefficient of the good, the distance between individuals, and the uptake rate of the external good. These variables join the coefficient of relatedness and the cost/benefit ratio in an expanded form of Hamilton's rule that includes both selfish and altruistic paths to the evolution of external goods strategies. This expanded framework can be applied to any external goods trait, and is a useful heuristic even when it is difficult to quantify the fitness consequences of producing the good.

The importance of 'eco-evolutionary feedbacks' in natural systems is currently unclear. Here, we advance a general hypothesis for a particular class of eco-evolutionary feedbacks with potentially large, long-lasting impacts in complex ecosystems. These eco-evolutionary feedbacks involve traits that mediate important interactions with abiotic and biotic features of the environment and a self-driven reversal of selection as the ecological impact of the trait varies between private (small scale) and public (large scale). Toxic algal blooms may involve such eco-evolutionary feedbacks due to the emergence of public goods. We review evidence that toxin production by microalgae may yield 'privatised' benefits for individual cells or colonies under pre- and early-bloom conditions; however, the large-scale, ecosystem-level effects of toxicity associated with bloom states yield benefits that are necessarily 'public'. Theory predicts that the replacement of private with public goods may reverse selection for toxicity in the absence of higher level selection. Indeed, blooms often harbor significant genetic and functional diversity: bloom populations may undergo genetic differentiation over a scale of days, and even genetically similar lineages may vary widely in toxic potential. Intriguingly, these observations find parallels in terrestrial communities, suggesting that toxic blooms may serve as useful models for eco-evolutionary dynamics in nature. Eco-evolutionary feedbacks involving the emergence of a public good may shed new light on the potential for interactions between ecology and evolution to influence the structure and function of entire ecosystems.

Many microbes cooperatively secrete extracellular products that favorably modify their environment. Consistent with social evolution theory, structured habitats play a role in maintaining these traits in microbial model systems, by localizing the benefits and separating strains that invest in these products from ‘cheater’ strains that benefit without paying the cost. It is thus surprising that many unicellular, well-mixed microalgal populations invest in extracellular toxins that confer ecological benefits upon the entire population, for example, by eliminating nutrient competitors (allelopathy). Here we test the hypotheses that microalgal exotoxins are (1) exploitable public goods that benefit all cells, regardless of investment, or (2) non-exploitable private goods involved in cell-level functions. We test these hypotheses with high-toxicity (TOX+) and low-toxicity (TOX-) strains of the damaging, mixotrophic microalga Prymnesium parvum and two common competitors: green algae and diatoms. TOX+ actually benefits from dense populations of competing green algae, which can also be prey for P. parvum, yielding a relative fitness advantage over coexisting TOX-. However, with non-prey competitors (diatoms), TOX- increases in frequency over TOX+, despite benefiting from the exclusion of diatoms by TOX+. An evolutionary unstable, ecologically devastating public good may emerge from traits selected at lower levels expressed in novel environments.

Biology needs a concept of individuality in order to distinguish organisms from parts of organisms and from groups of organisms, to count individuals and compare traits across taxa, and to distinguish growth from reproduction. Most of the proposed criteria for individuality were designed for ‘unitary’ or ‘paradigm’ organisms: contiguous, functionally and physiologically integrated, obligately sexually reproducing multicellular organisms with a germ line sequestered early in development. However, the vast majority of the diversity of life on Earth does not conform to all of these criteria. We consider the issue of individuality in the ‘minor’ multicellular taxa, which collectively span a large portion of the eukaryotic tree of life, reviewing their general features and focusing on a model species for each group. When the criteria designed for unitary organisms are applied to other groups, they often give conflicting answers or no answer at all to the question of whether or not a given unit is an individual. Complex life cycles, intimate bacterial symbioses, aggregative development, and strange genetic features complicate the picture. The great age of some of the groups considered shows that ‘intermediate’ forms, those with some but not all of the traits traditionally associated with individuality, cannot reasonably be considered ephemeral or assumed transitional. We discuss a handful of recent attempts to reconcile the many proposed criteria for individuality and to provide criteria that can be applied across all the domains of life. Finally, we argue that individuality should be defined without reference to any particular taxon and that understanding the emergence of new kinds of individuals requires recognizing individuality as a matter of degree.

Altruistic suicide is best known in the context of programmed cell death (PCD) in multicellular individuals, which is understood as an adaptive process that contributes to the development and functionality of the organism. After the realization that PCD-like processes can also be induced in single-celled lineages, the paradigm of altruistic cell death has been extended to include these active cell death processes in unicellular organisms. Here, we critically evaluate the current conceptual framework and the experimental data used to support the notion of altruistic suicide in unicellular lineages, and propose new perspectives. We argue that importing the paradigm of altruistic cell death from multicellular organisms to explain active death in unicellular lineages has the potential to limit the types of questions we ask, thus biasing our understanding of the nature, origin, and maintenance of this trait. We also emphasize the need to distinguish between the benefits and the adaptive role of a trait. Lastly, we provide an alternative framework that allows for the possibility that active death in single-celled organisms is a maladaptive trait maintained as a byproduct of selection on pro-survival functions, but that could-under conditions in which kin/group selection can act-be co-opted into an altruistic trait.

Organisms from prokaryotes to plants and animals make costly investments in diffusible beneficial external products. While the costs of producing such products are born only by the producer, the benefits may be distributed more widely. How are external goods-producing populations stabilized against invasion by nonproducing variants that receive the benefits without paying the cost? This question parallels the classic question of altruism, but because external goods production need not be altruistic per se, a broader range of conditions may lead to the maintenance of these traits. We start from the physics of diffusion to develop an expression for the conditions that favor the production of diffusible external goods. Important variables in determining the evolutionary outcome include the diffusion coefficient of the good, the distance between individuals, and the uptake rate of the external good. These variables join the coefficient of relatedness and the cost/benefit ratio in an expanded form of Hamilton's rule that includes both selfish and altruistic paths to the evolution of external goods strategies. This expanded framework can be applied to any external goods trait, and is a useful heuristic even when it is difficult to quantify the fitness consequences of producing the good.

[1] Many dendroclimatic studies have been conducted in Alaska to understand recent climate changes, identify past and current warming trends, and determine how climate change may influence ecosystems. Four new white spruce (Picea glauca [Moench] Voss) ring-width chronologies from four sites along a 30 kilometer north-south transect in the Lake Clark National Park and Preserve on the Alaskan Peninsula span a common interval from AD 1769 to 2003. Two sites show an internally consistent positive growth response to increasing April–July temperatures after 1950. The two other sites each contain two subpopulations showing varying growth responses. One subpopulation diverges from historical temperature data after 1950 and one shows increased growth consistent with warming or exceeds expected growth increases. The growth decline may be due to temperature-induced drought stress that acts on some trees. Unprecedented climatic changes are triggering diverse growth responses between and within study sites that may greatly complicate dendroclimatic reconstructions of past climate conditions.